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J Autism Dev Disord (2009) 39:1603–1607

DOI 10.1007/s10803-009-0786-4

BRIEF REPORT

Brief Report: Inhibitory Control of Socially Relevant Stimuli


in Children with High Functioning Autism
Hilde M. Geurts Æ Sander Begeer Æ Lex Stockmann

Published online: 19 June 2009


Ó The Author(s) 2009. This article is published with open access at Springerlink.com

Abstract The current study explored whether inhibitory Introduction


control deficits in high functioning autism (HFA) emerged
when socially relevant stimuli were used and whether One of the most influential cognitive theories of autism
arousal level affected the performance. A Go/NoGo para- spectrum disorders (ASD) highlights the primary role of
digm, with socially relevant stimuli and varying presenta- deficits in executive functions (Geurts et al. 2009; Hill
tion rates, was applied in 18 children with HFA (including 2004; Pennington and Ozonoff 1996; Russell 1997), the
children with autism or Asperger syndrome) and 22 typi- cognitive control processes that guide the ability to monitor
cally developing children (aged 8–13 years). Children with ongoing performance in a dynamically changing environ-
HFA did not show inhibitory control deficits compared to ment. Within social interactions it is necessary to select and
the control group, but their performance deteriorated in the initiate complex behaviors in response to the specific
slow presentation rate condition. Findings were unrelated necessities of the social environment (Bachevalier and
to children’s abilities to recognize emotions. Hence, rather Loveland 2006). Hence, the ability to generate appropriate
than a core deficit in inhibitory control, low arousal level in responses during social interactions involves selecting the
response to social stimuli might influence the responses most fitting response while inhibiting those responses
given by children with HFA. deemed inappropriate which is an important aspect of
executive functioning. Despite its suggested relevance to
Keywords Autism  Arousal  Emotion  social functioning, executive functions are mainly studied
Inhibitory control  Executive functions in non-social domains (Hill 2004), using tasks that focus on
specific, elementary abilities such as planning behaviour
and inhibitory control (Sergeant et al. 2002). Findings on
inhibitory control in ASD are particularly mixed, with
multiple reports on both deficits (e.g., Christ et al. 2007;
Geurts et al. 2004, 2008; Solomon et al. 2008), and
H. M. Geurts (&) attainments (e.g., Christ et al. 2007; Happé et al. 2006;
Department of Psychonomics, University of Amsterdam,
Kana et al. 2007; Ozonoff and Jensen 1999; Raymaekers
Roetersstraat 15, 1018 WB Amsterdam, The Netherlands
e-mail: h.m.geurts@uva.nl et al. 2007; Schmitz et al. 2006), which may in part be due
to differences in arousal modulation (Liss et al. 2006;
S. Begeer Raymaekers et al. 2004). The current study will focus on
Department of Developmental Psychology, VU University,
the role of arousal modulation in the inhibitory control of
Amsterdam, The Netherlands
socially relevant stimuli of children with ASD.
L. Stockmann Over-arousal, attained by fast presentation rates of
Center for Autism, Oestgeest, The Netherlands stimuli, can cause inhibitory control deficits in participants
with ASD (Raymaekers et al. 2004; Sanders 1998). How-
Present Address:
H. M. Geurts ever, when non-social stimuli are used, these deficits are
Dr. Leo Kannerhuis, Doorwerth, The Netherlands not always found in children with ASD, even when fast

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presentation rates were used (e.g., Christ et al. 2007; Happé Table 1 Controls and HFA: group means and standard deviations for
et al. 2006; Kana et al. 2007; Raymaekers et al. 2007; age, IQ, and, rating scales
Schmitz et al. 2006). The role of arousal modulation in Measure Group
inhibitory control tasks may be more clear when social
Controls (n = 22) HFA (n = 18)
stimuli are used, e.g., emotional faces, which are known to
elicit both hypo- and hyper-responsiveness in children with Gender (Boys/Girls) 19/3 16/2
ASD, likely due to impaired arousal modulation (Baker M SD M SD Group
et al. 2008; Bolte et al. 2008; Corden et al. 2008a, b; comparison
Rogers and Ozonoff 2005; Schoen et al. 2008). (p)
In the current study, we investigated inhibitory control Age 10.3 1.4 10.3 1.6 .96
deficits in children with ASD when processing socially
FSIQ 103.2 24.1 108.0 19.0 .50
relevant stimuli. Children with high functioning autism
CCC
(HFA, including children with autism and with Asperger
Speech Output 34.0 2.7 33.9 3.1 .91
syndrome) were compared to typically developing control
Syntax 31.5 0.9 31.6 0.7 .74
children on two experimental tasks: (a) a Go/NoGo-task
Inappropriate Initiation 28.2 1.8 24.1 3.0 \.001
with emotional stimuli presented at two different presen-
Coherence 34.8 1.8 30.0 3.2 \.001
tation rates; and (b) an emotion recognition task to deter-
Stereotyped Conversation 28.5 1.8 21.6 3.8 \.001
mine whether children with HFA have deficits in the
Use of Conversational 30.4 1.4 23.8 2.8 \.001
recognition of simple emotions. We hypothesized a limited Context
ability to inhibit responses to social stimuli in children with
Conversational Rapport 32.3 2.0 26.5 2.9 \.001
ASD compared to controls. Furthermore, we explored the
Social Relationships 33.0 1.2 27.4 2.6 \.001
effect of the presentation rate (i.e., arousal level) on the
Interests 31.2 1.7 26.2 3.0 \.001
ability to inhibit the prepotent motor response to these
CSBQ
socially relevant stimuli.
Not optimally tuned 3.7 3.6 12.2 4.5 \.001
Reduced social contacts 1.6 3.0 9.6 3.6 \.001
Orientation problems 1.2 1.9 6.9 3.5 \.001
Methods
Problems in understanding 1.5 1.4 8.7 3.5 \.001
Stereotype behavior 0.6 1.1 4.6 3.1 \.001
Participants
Resistance to change 0.2 0.5 3.2 3.1 \.001
Total score 9.0 8.2 45.3 11.2 \.001
Twenty-two children with HFA and 22 typically develop-
ing control children participated in this study. Participants Note. CCC, children’s communication checklist, CSBQ, Children’s
with HFA fulfilled established diagnostic criteria according Social Behavior Questionnaire, FSIQ, full scale IQ, HFA, high
to the DSM-IV-TR (American Psychiatric Association functioning autism (including children with a diagnosis of autism and
Asperger syndrome, see text)
2000), as well as the autism algorithm cut-offs on two
Note that the lower the score on the CCC, the more impaired the child
questionnaires that assess the defining social problems of
is, while in the CSBQ a higher score indicates impairment
children with HFA: Children’s Communication Checklist
(CCC, Bishop 1998) and the Children’s Social Behavior
Questionnaire (CSBQ, Luteijn et al. 2002). Three children g2 = .00, FSIQ, F(1, 40) \ 1, ns, g2 = .01, and gender, v2
were excluded from the study because they had an esti- (1, N = 40) = .058, ns. As expected, the parents of the
mated IQ below 75 as measured by the short version of the children with HFA reported more problems when com-
Dutch Wechsler Intelligence Scale for Children (WISC-III; pared to typically developing children on all scales of the
de Kort et al. 2002). One child refused to do all the tests. CCC and the CSBQ (see Table 1). The parents of the
Therefore, eventually 18 children with a clinical diagnosis control children indicated that none of these children, or
of autism (n = 7) or Asperger Syndrome (n = 11) aged their siblings, was known with behavioural problems or a
8–13 years participated in this study. One participant with psychiatric or neurological diagnosis.
HFA was on methylphenidate, but discontinued medication
at least 20 h before testing allowing for a complete wash- Material
out. None of the other children used any kind of
medication. Emotional inhibition task. In line with Raymaekers et al.
All children had an estimated IQ above 75 (range HFA: (2004; 2007) the inhibition task was a Go/NoGo paradigm
82–144; range controls: 75–154). The two groups did not with two types of trials: Go-trials and NoGo-trials. In the
differ from each other with respect to age, F(1, 40) \ 1, ns, middle of the computer screen there was a small square as

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constant fixation point. On each trial a visual stimulus, (Lundqvist et al. 1998) were used, which were similar to
either a face with a happy expression (Go-trial) or a face the type of stimuli used in the emotional inhibition task.
with an angry expression (NoGo-trial) appeared for The task consisted of 80 trials of 16 different faces, half of
300 ms. In a Go-trial, the participants were instructed to which displaying a happy emotion, the other half display-
press a response key with their index finger of their dom- ing an angry emotion.
inant hand if a face with a happy expression appeared,
whereas in a NoGo-trial, participants had to refrain from Procedure
responding if a face with an angry expression appeared. To
enhance the ecological validity of the emotional stimuli we After the parents filled out both questionnaires and written
chose emotions that promote approaching behavior in the informed consents were obtained, the participants were
Go-trial (happy expressions), and emotions that promote tested. Within the inhibition task the order of two presen-
aversive behavior in the NoGo-trial (angry expressions, tation rates were counterbalanced across the participants.
Frijda 1986; Isen 1987). Eight different faces were used as The emotional decision task was always administrated last
stimuli, taken from the Karolinska Directed Emotional to prevent cross-over effects. All participants received a
Faces set which consists of 4,900 pictures of human facial small gift at the end of the test session and the parents or
expressions (Lundqvist et al. 1998). The set contains 70 caregivers were sent reports of the overall findings of the
actors (35 male, 35 female; age range 20–30 years) each study.
displaying seven different emotional expressions. In our
selection there were equal numbers of men and women, all
wearing the same plain blue–grey t-shirt and each person Results
was shot once looking happy and once looking angry.
There were two conditions within this task, a fast pre- Mean reaction time and intrasubject variability (arousal).
sentation rate (determined in a pilot study and following All children were faster and less variable in the fast pre-
Raymaekers et al. 2007), using a 2 s interstimulus interval sentation rate compared to the slow condition, respectively
(defined in terms of onset to offset) and a slow presentation F (1, 38) = 74.07, p \ .001, g2 = .66 and F (1, 38) =
rate, using a 6 s interstimulus interval. To keep the time on 10.00, p \ .005, g2 = .21. In their overall performance
task effect equal for both conditions, the fast condition children with HFA could not be differentiated from control
consisted of 200 trials (160 Go-trials and 40 NoGo-trials) children on response speed, F (1, 38) = 2.59, ns, g2 = .06,
and the slow condition consisted of 80 trials (64 Go-trials however, the responses of the children with HFA were
and 16 NoGo-trials). So in each condition 20% of the trials more variable than the control children, F (1, 38) = 4.09,
were NoGo-trials. The participants started with 20 practice p \ .05, g2 = .10. A Group * Presentation rate interaction,
trials. In these practice trials other faces were used than in F (1, 38) = 7.00, p \ .02, g2 = .16 (see Table 2), indi-
the experimental trials. The duration for each condition, cated a different effect of presentation rate on response
including instructions and practicing, was *10 min. speed in HFA and controls. While the fast presentation rate
Hence, without instructions the condition with the 2 s elicited similar mean reaction times in both groups (ns), the
interstimulus interval lasted 7.6 min, while the 6 s condi- slow presentation rate elicited slower responses in the HFA
tion lasted 8.4 min.
The individual mean reaction times of correct Go-trials
were calculated. Second, the intrasubject variability (stan-
Table 2 Group means and standard deviations for the emotional
dard deviation of the mean reaction time of correct Go- inhibition task for controls and participants with HFA
trials) was calculated as this is also linked to arousal
modulation (Raymaekers et al. 2004, 2007). Third, the Measure Group
percentage of errors was calculated for each individual. Controls HFA
The percentage of errors is the number of commission Fast Slow Fast Slow
errors (the participant responded to a NoGo-trial) divided (2 s ISI) (6 s ISI) (2 s ISI) (6 s ISI)
by the total number of NoGo-trials. Typically, deficient
M SD M SD M SD M SD
inhibitory control leads to an increased error rate on NoGo-
trials (Casey et al. 1997). MRT 446.6 80.3 510.6 87.6 476.2 129.4 597.0 168.3
Emotion recognition task. In this task the participants SD MRT 125.7 42.33 134.2 45.2 151.2 63.0 183.1 90.0
had to decide whether the person on the picture displayed a % Errors 10.3 6.0 10.2 5.4 12.7 5.1 11.3 5.0
happy or an angry emotion by pushing one of two buttons, Note. HFA, high functioning autism (including children with a
namely a blue one for happy and a red one for angry. diagnosis of autism and Asperger syndrome, see text), ISI, inter
Stimuli from the Karolinska Directed Emotional Faces set stimulus interval, MRT, mean reaction time, SD, standard deviation

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than in the control group, p \ .05. There was no differ- or to keep a sufficient amount of motivation. We tried to
ential effect of presentation rate on intrasubject variability eliminate sustained attention as a confounding factor to
for the two groups, F (1, 38) = 3.36, ns, g2 = .08. keep the time on task exactly the same in both presentation
Percentage errors (inhibitory control): All children made rate conditions and by counterbalancing this presentation
less errors when the presentation rate was slow than when the rate (see also Christ et al. 2007). However, it is still pos-
presentation rate was fast, F (1, 38) = 6.96, p \ .02, sible that the children with HFA were less motivated and
g2 = .16, but no Group, F \ 1, ns, g2 = .01, nor interaction put in less effort when the presentation rate was slow.
effects, F (1, 38) = 1.08, ns, g2 = .03, were found. Whether this is especially the case when socially relevant
There were no group differences in the recognition of stimuli are used needs to be studied in future research.
happy or angry faces on the emotion recognition task Although one might interpret these findings as evidence for
(Response speed: Group, F (1, 38) = 2.88, ns, g2 = .07; under-arousal in children with HFA when confronted with
Group * Emotion, F (1, 38) = 2.52, ns, g2 = .06: Accu- facial expressions, we believe that replication studies (in
racy: Group, F (1, 38) = 1.18, ns, g2 = .03, Group which psycho physiological measures, such as heart rate
* Emotion, F \ 1, ns, g2 = .02.). variability or skin conductance, of arousal are included; see
also Geurts et al. 2009) are needed before such a conclu-
sion can be drawn.
Discussion A potential confound of the experimental set up might
be the choice to include emotions with response tendencies
The current results suggest that children with HFA are able in line with the requested action in the emotional inhibition
to exert adequate inhibitory control when processing facial task. However, reversing the instruction by requesting
expressions, which is in line with most former studies that responses to angry expressions and no responses to happy
used neutral stimuli (e.g., Christ et al. 2007; Happé et al. expressions could introduce an additional inhibition ele-
2006; Kana et al. 2007; Raymaekers et al. 2007; Schmitz ment to the task, above the inhibitory control that is
et al. 2006). Despite their equal accuracy, children with inherent to the Go/NoGo-task. Moreover, this is not likely
HFA responded disproportionably slower than controls in to explain the current findings.
the slow, but not in the fast presentation rate condition. In sum, we show that even when more socially relevant
This slowness is generally not related to inhibitory control stimuli are used children with HFA do not show inhibitory
deficits per se (Casey et al. 1997), and could not be control deficits. However, motivation and/or arousal might
attributed to the inability to recognize simple emotions. In be a factor that influences the processing of socially rele-
line with Raymaekers et al. (2004) we found that presen- vant stimuli as slow presentation rates resulted in more
tation rate affected children with HFA differently than profound performance decrements in children with HFA as
typically developing children, however, our pattern of compared to typically developing children. How and when
findings differs from the earlier reported pattern. Ray- motivation plays a role in children with HFA needs to be
maekers et al. (2004) showed that on a neutral inhibitory addressed in future research as this might give us insight in
control task adults with ASD were more impaired (as how we can motivate children with HFA in such a way that
reflected by accuracy measures) when the presentation rate in daily life their performances increase.
was fast, while we found that children with HFA were
more impaired when the presentation rate was slow (as Acknowledgments We want to thank all the parents and children
that participated in the current study and Channa Hijmans and Mir-
reflected by response speed measures). Among others, the eille Visser-Klaver for testing the participating children. We want to
two studies differed in the timing of the fast presentation thank Mark Rotteveel for introducing us to the Karolinska Directed
rates and in the age of the participants. In a study in chil- Emotional Faces set.
dren with HFA, with a similar fast presentation rate as in
Open Access This article is distributed under the terms of the
the current study, Raymaekers et al. (2007) could not Creative Commons Attribution Noncommercial License which per-
replicate the former adult pattern of findings (Raymaekers mits any noncommercial use, distribution, and reproduction in any
et al. 2004). This suggests that the effect of presentation medium, provided the original author(s) and source are credited.
rate is both age and stimulus dependent, as in children the
presentation rate only seems to influence performance
when emotional stimuli are used.
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